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Czech J. Food Sci. Vol. 23, No. 3: 85–92

Prospects for Rapid Bioluminescent Detection Methods in the Food Industry – a Review

PAVEL DOSTÁLEK and TOMÁŠ BRÁNYIK

Department of Fermentation Chemistry and Bioengineering, Faculty of Food and Biochemical Technology, Institute of Chemical Technology Prague, Prague, Czech Republic

Abstract

DOSTÁLEK P., BRÁNYIK T. (2005): Prospects for rapid bioluminescent detection methods in the food industry – a review. Czech J. Food Sci., 23: 85–92.

This review surveys rapid bioluminescent detection techniques applied in food industry and discusses the historical development of the rapid methods. These techniques are divided into two groups: methods based on bioluminescent (ATP) assay, and on bacterial bioluminescence. The advantages and disadvantages of these methods are described. The article provides the bibliography of fluorescent method applications in food samples.

Keywords: bioluminescence; ; ATP; food samples; food industry; food safety; microbiological techniques

Current trends in nutrition and food technology and controlled in the course of preparation and impose increasing demands on food microbiol- packing of the product are designated as Critical ogists to ensure a safe food supply (GRIFFITHS Control Points (CCP). The general categories of 1993). The last 25 years have been dedicated to the hazards include: and their toxic development of new methods for Quality Assur- products; Chemicals such as toxins, heavy metals ance, Total Quality Management and the Hazard and pesticide residues, and Foreign Matter (CURTIS Analysis and Critical Control Point (HACCP) & HUSKEY 1974). systems (UGAROVA et al. 1993). The HACCP sys- Although the most effective methods of monitor- tem was devised as a procedure to ensure the ing CCP are often physical or chemical, many of safety and quality of food products (JACKSON & the hazards associated with the food production SHINN 1979). It was developed by the U.S. Food are of microbiological nature. Microorganisms of and Drug Administration (FDA) for regulating and concern to food manufacturers can be divided into inspecting food plants (BAUMAN 1974). The basic two groups: (i) the pathogens and (ii) those that premise is to identify possible hazards in advance can be used as indicator . It is clear that and set up a system of procedures, inspections, any direct test for microorganisms must be rapid and records to minimise the possibilities of the enough to be compatible with HACCP and it is hazards causing unsafe or off-quality end products. imperative, therefore, to quit the traditional use of The points at which hazards might be encountered media and plates (KODIKARA et al. 1991). Of the

Supported by the Ministry of Foreign Affairs and Hebrew University (Israel) and by the Ministry of Education, Youth and Sports of the Czech Republic, Project No. MSM 6046137305.

85 Vol. 23, No. 3: 85–92 Czech J. Food Sci. emerging technologies for rapid microbiological 100 fg/CFU in yeasts (LEACH & WEBSTER 1986; analysis, bioluminescence is purported to be the GIROTTI et al. 1997; CROSS 1992). technique giving results in the shortest time. The distinct areas of bioluminescence that are of use in Disturbing factors the food industry are: ATP bioluminescence and bacterial bioluminescence (FUNG 2002). Almost all food products contain nonmicrobial sources of “intrinsic” or “somatic” ATP which must BIOLUMINESCENT ADENOSINE be eliminated by sample pretreatment procedures. TRIPHOSPHATE (ATP) ASSAY Somatic cells have to be lysed and incubated with the apyrase or somase (ATPase) to de- All living cells contain intracellular ATP needed stroy the released ATP. After this treatment, the for the regulation of the stored metabolic energy, microorganisms are chemically disrupted and for the maintenance of the enzyme systems, and the released microbial ATP is determined using for biosynthesis of cellular constituents during all purified - reagent. Another pos- phases of growth. Storage at suboptimal conditions sibility for avoiding somatic ATP interference is to may reduce the intracellular ATP levels. In dead physically separate microorganisms from somatic cells, ATP is broken down by autolysis within a cells by differential filtration, combinations of few minutes. ATP can thus be used as a measure exchange resins, centrifugation and filtration, or of microbial . Indeed, linear relationships enzymatic destruction of somatic ATP followed by have been found between intracellular ATP levels differential filtration procedures (CROSS 1992). and total number of colony-forming units (CFU) Quenching of emitted is another factor that with bacteria as well as with yeasts. can adversely affect microbial ATP determination. A very rapid and sensitive ATP assay, based Certain compounds from the food samples can on the ( pyralis) ATP lumines- strongly reduce the amount of light measured cent reaction, was developed as an alternative to photometrically. Internal standards must then the traditional plate count techniques in routine be incorporated in the dilutions to be tested, as microbiological analysis of food and beverages has been shown with skimmed milk. Some food (LEACH & WEBSTER 1986). samples may also contain inhibitory substances catalyses the ATP-dependent influencing the luciferase activity (LEACH & WEB- oxidative decarboxylation of luciferin (LH2) re- STER 1986). sulting in the production of light as shown in the reaction (where P denotes the product oxyluciferin APPLICATION OF THE ATP ASSAY and hν denotes the light produced): IN THE FOOD INDUSTRY Mg2+ (LH2) + ATP + O2 P + AMP + PPi + CO2 + hν Hygiene monitoring

Three factors led to a greater utilisation of biolu- Probably the most widely used current applica- minescent methods for analysis in the 1980s (LEACH tion of ATP bioluminesce in the food industry is & WEBSTER 1986), i.e. (1) the availability of com- that for the estimation of surface cleanliness. The mercially prepared reagents, (2) the commercial total amount of ATP present on a surface can be manufacture of suitable measuring instruments, extracted through swabbing and assayed extremly and (3) the holding of conferences and the publish- rapidly (i.e. within 5 min) with no less accuracy ing of reports and monographs that highlight the than that obtained using traditional techniques. advantages of bioluminescent techniques (LEACH The result indicates the overall contamination of & WEBSTER 1986). the surface because ATP from all microbial sources Commercially available manual or automated will be detected. The amount of contamination –13 luminometers can detect less than 0.1 pg (or 10 g) determined by ATP and plate count methods cor- of ATP per cuvette, corresponding to approximately related well in about 80% of samples (POULIS et al. 100 bacterial cells. Quantitation of the steady-state 1993). A number of bioluminescent-based hygiene ATP levels in a variety of microorganisms revealed monitoring kits are commercially available (Lumac ATP ranges from 0.1 to 4.0 fg/CFU (average ca. Hygiene Monitoring Kit, Lumac Water Microbial –15 1 fg or 10 g/CFU) in bacteria and from 10 to Kit) and are used routinely to monitor critical

86 Czech J. Food Sci. Vol. 23, No. 3: 85–92 points in many food processing operations world- lent to 105 to 108 CFU/g (based on an ATP content wide (ANONYM 1996). of 1 fg/CFU). A successful application of the ATP assay, therefore, depends on a proper pretreat- Milk and milk products ment procedure (BASOL & GOGUS 1996). In this case, the lower detection limit was 5 × 104 CFU/g, ATP bioluminescent methods can be used for and good correlations between ATP content and monitoring raw milk quality from the point of colony counts were found. Good correlations also view of somatic cell count and microbial count. exist between ATP content and colony counts in An indication of the somatic cell concentration vacuum-packed cooked cured meat products. Many in milk can be obtained from the concentration cooked meat products appear to contain relatively of ATP in milk following the treatment with non- low contents of somatic ATP. The removal of this ionic detergent (WEBSTER et al. 1988). This can somatic ATP is therefore not necessary, and as a be used as an index for mastitis infection. Recent consequence, the assay time can be reduced to less ATP bioluminescent procedures can be used to than 5 min. The detection limit is 105–106 CFU/g, detect as few as 104 CFU/ml of bacteria in milk which suffices for screening these vaccum-packed in 5 to 10 min. This makes the technique useful cooked cured meat products (BAUTISTA et al. as a rejection test for the incoming milk tankers 1994, 1995; SIRAGUSA & CUTTER 1995; RUSSEL at milk processing plants (GRIFFITHS & PHILLIPS 1995). A commercial kit also exists for checking 1989; MOORE et al. 2001). These tests are avail- the microbial quality of raw meat in 30 min – the able commercially (ANONYM 1996) and marketed Lumac Meat Microbial Kit (ANONYM 1996). by Biotrace (Bridgen, Wales) and Lumac (Laand- graaf, the Netherlands – Raw Milk Microbial Kit). Carbonated beverages and fruit juices ATP bioluminescent methods can also be used for pasteurised milk quality and sterility testing Many carbonated beverages are readily filterable of UHT and other dairy products. Because ATP and contain low or undetectable levels of somatic is an integral part of the metabolism of bacte- ATP. Simple filtration procedures are sufficient rial cells, the concentration of ATP may provide for detecting low levels of yeasts (5 CFU/ml) by a better indication of the activity of lactic acid ATP assay. Fruit juices, however, contain high lev- bacteria for monitoring starter culture activity els of somatic ATP and many methods exist for then the measurement of pH changes. A strong the pretreatment. It has been concluded that the correlation between the acid production and ATP bioluminescent ATP assay offers opportunities for concentration exists for a number of lactic acid quality control of fruit juice: detection limits are bacteria, including Lactococcus lactis and Lacto- 103 CFU/ml for yeasts and 105 CFU/ml for bacteria bacillus acidophilus, during their growth in milk. (UGAROVA et al. 1993). A commercial kit is avail- The monitoring of the change in ATP during the able from Lumac which checks fruit juice sterility. growth in milk rapidly indicated the presence of After a short preincubation period, the presence of antibiotic residues or phage (GRIFFITHS 1993). microorganisms is tested using a bioluminescent Concentrations as low as 0.005 U/ml of penicillin technique. The Lumac Beer Microbial Kit is spe- can be detected in about 90 min. An interesting cifically designed for the rapid detection of micro- application of is emerging that will bial contamination or its absence in finished beers have implications for the dairy industry in the (ODEBRECHT et al. 2000). The results are obtained future, namely the development of biolumines- within 20 hours which is faster in comparison to cent assays for detecting a variety of and conventional techniques (ANONYM 1996). other substances of importance in this industry (GRIFFITHS 1993). BACTERIAL BIOLUMINESCENCE

Meat and meat products (those capable of emitting light) are classified into four major genera: , The estimation of the microbial load on meat by , Alteromonas, and Xenorhabdus. an ATP bioluminescence assay is also hampered The bioluminescent reaction, catalysed by the by interfering somatic ATP. The ATP background enzyme luciferase, involves the oxidation of a long- levels in meat samples, for example, may be equiva- chain aldehyde and reduced riboflavin phosphate

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(FMNH2) and results in the emission of blue green destruction, monitoring starter culture integrity, light (BAKER et al. 1992). biocide and virucide challenges, and studying the recovery of sublethally injured cells (BAKER et al. luciferase FMNH2 + O2 + RCOH FMN + RCOOH + 1992; HILL et al. 1993; MEIGHEN 1993).

H2O + light (490 nm) Detection of specific bacterial pathogens The primary source of energy for the light is sup- and indicator organisms plied by the conversion of the respective aldehyde to the corresponding fatty acid. Long-chain alde- At present, in food laboratories the determina- hydes are essential for the luminescence reaction tion of ATP by firefly luciferase is used to detect and the aldehyde tetradecanal appears to be the and enumerate cells, and to assess the shelf life natural substrate for the luminescence reaction. and microbial quality of many kinds of food. The

The reaction is highly specific for FMNH2 which ATP assay is a rapid technique but, for the time is formed by the reaction: being it lacks specificity for the identification of bacteria. This specificity can be achieved with lux FMN oxidoreductase NAD(P)H + FMN FMNH2 genes from . Lux genes can be introduced into , which will then be Thus, the luciferase reaction may be driven by absorbed by specific bacteria thus transfering the coupling it to any system that produces FMNH2 light-emitting genes to those bacteria (KODIKARA (GIROTTI et al. 1990, 1993a; COULET & BLUM et al. 1991). By knowing what type of bacteria one 1992; GIROTTI 1993b; SAUL et al. 1996; MICKOVÁ wishes to detect, it is only the matter of obtaining et al. 2004; NIVENS et al. 2004). the host specific phages for that particular organ- ism and performing genetic manipulations. The Applications of lux gene technology organisms are mixed with the phages and the light in food microbiology emissions can be quantitatively measured. The re- search has shown that the bioluminescent assay is In a review of the potentials of in vivo biolu- rapid (usually less than 1 h), sensitive (luminometers minescence in microbiology, STEWART (1990) can detect as few as 500 bacteria), simple, specific, states that there are three components necessary and demonstrates a good correlation between cell for novel developments in gene technology. The numbers and bioluminescence (STEWART 1990; first one is the potential of a high level of the light STEWART & WILLIAMS 1992; REES et al. 1995). output from individual cells. The second one is Dark terrestrial organisms that need to be moni- the rapidly expanding ability to transfer the bio- tored in food microbiology (pathogens, starter chemistry of the light production by cloning lux cultures, hygiene indicators) lack the ability to gene vectors into normally dark microorganisms. produce luciferase or fatty acid reductase, but they

The third component involves the use of instru- can supply FMNH2. Therefore, all that is needed ments, originally designed for in vitro ATP assays, is the transfer of luciferase genes and, in some which permit the detection of light from only a cases, fatty acid reductase. Phage P22 is a nar- few hundred bacteria per ml. All of these are im- row host range phage infecting only Salmonella portant in implementing bacterial bioluminescent typhimurium. After infection with this phage, assays into the realm of microbiological testing. as few as 100 cells of S. typhimurium could be Whereas a number of ATP luminescent techniques detected in 50 min by monitoring light emission. are presently employed in various aspects of food Lux containing bacteriophages should be able to microbiology, the application of bacterial biolumi- target other pathogens, such as Campylobacter nescence is still at the research or prototype levels. spp. and Listeria monocytogenes. There may still Many experiments have been and are currently be a need for the recovery and enrichment pro- made, to determine the feasibility and usefulness cedures prior to phage detection, because of zero of the assays proposed. Some of the applications tolerance (regulatory requirements) for L. mono- for the use in the food industry include the detec- cytogenes. However, due to the sensitivity (100 per tion of specific bacterial pathogens and indicator ml) and specificity of the host and the phage, the microorganisms, on-line monitoring of hygiene enrichment time can be short providing simple quality, determining the effectiveness of spore same day testing for pathogenic bacteria.

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Enteric bacteria are used in the food industry as disinfectants. Materials such as food waste, organic indicators of poor sanitary conditions. Lux genes soil, dust and organisms can neutralise biocide have been inserted into phages that infect a broad activity without reducing the apparent chemical range of enteric bacteria providing a reagent for activity. For this reason, the monitoring of biocide an on-line hygiene test with a detection limit of levels is essential to provide an adequate protec- 1000 enterics per g or per cm2. After a 4-h en- tion. Current testing techniques (dipslides, dye richment of the sample, viable enteric counts of reduction tests, microbial challenge tests) require 10 per g or per cm2 can be distinguished from the more than 18 h and are thus not suitable for on- background (KODIKARA et al. 1991; BAKER et al. site evaluation. Bioluminescent microorganisms 1992; WADDELL & POPPE 2000). offer the potential for rapid biocide testing. The test takes only 10–15 min and provides a good Sporeforming organisms correlation with the viable count evaluation. Since and bioluminescence dead cells produce no light, the biocidal effect is measured as a decrease in the light emission of Bacterial luciferase can function in gram-positive the luminescent culture. This method has been organisms, although it originates from gram-negative used to test the effectiveness of certain biocides on ones. Bacillus spp. are capable of producing heat L. monocytogenes with good results after 15 min ex- stable dormant endospores (COOK et al. 1993). The posure. Assessing antiviral activity usually requires spores obtained from phenotypically bioluminescent cell culture work or electron microscopy facilities. vegetative cells are dark. When the spores germinate, A rapid bioluminescent test has been developed by the onset of electron transport and the initiation inserting lux A and lux B genes into λ phage. After of metabolism are the early events. With the lux the exposure to hypochlorite (virucidal agent), the containing spores, germination is accompanied by lux+ phages were unable to infect a nonlumines- the of bioluminescence. This provides a cent E. coli (ULITZUR 1986b; STEWART et al. 1991; sensitive, real-time monitoring of the germination and THOMULKA et al. 1992; FABRICANT et al. 1995). growth processes. The spores that have been killed or injured, and are thus unable to germinate, produce Recovery of sublethally injured cells no light (BAKER et al. 1992; HILL et al. 1993). Sublethal injury refers to the state where a micro- Lactic acid bacteria and starter cultures is neither actively growing nor biochemi- cally dead. Microorganisms in this state may arise Many assays based on luminescent bacteria are in food after heating, chilling, freezing, moisture used in the dairy industry. The presence of bacte- reduction, irradiation, or exposure to preservatives. riophages or antibiotics can cause starter culture Sublethally injured cells can retain their pathogenic failure in cheese or yoghurt manufacture. Biolu- traits, which makes enumeration of these cells minescent lactic-acid streptococci are suitable during microbial analysis very important. They for use as an indicator of the presence of lytic usually need a period for the intracellular repair. It phages or antibiotics. This light-emitting com- is possible to monitor with sensitive luminometers ponent of starter cultures can be monitored for a the recovery of sublethally injured cells back to loss of luminescence that indicates the presence optimum bioluminescence levels without having of an inhibitory substance. Using a luminescent to observe a single cell division. For example, using derivative of Lactobacillus casei, the technique a bioluminescent recombinant strain of S. typh- allowed the detection of penicillin G to levels as imurium, researchers have shown that 20% of the low as 0.03 µg/ml (0.05 units/ml) in 30 min, and population can survive a freeze/thaw cycle with the bacteriophages at concentrations as low as 105/ml biochemical system sufficiently intact to permit in 100 min (ULITZUR 1986a; BAKER et al. 1992; immediate and sustained bioluminescence. By GRIFFITHS 1993). classical plate techniques, only 2.5% of the original inoculum could be detected. This has important Effectiveness of biocides and virucides implications for the food industry as these results suggest that appreciable numbers of toxigenic cells, Biocides are used for the microbiological con- that are not considered viable by conventional trol in food manufacturing or as preservatives or enumeration techniques, may continue to produce

89 Vol. 23, No. 3: 85–92 Czech J. Food Sci. toxigenic compounds after processing (ELLISON bioluminescent assays. The resurgence of interest et al. 1994; DUFFY et al. 1995). in ATP (firefly) bioluminescence and the dramatic improvements in the reagent quality and instru- ADVANTAGES AND DISADVANTAGES ment sensitivity has led to the availability of ap- OF THE LUMINESCENT ATP ASSAY plications of direct relevance to many branches AND BACTERIAL LUMINESCENT SYSTEM of the food industry, and many kits are now com- IN FOOD MICROBIOLOGY mercially available. The many advantages of assays using bacterial The ATP bioluminescent assay is very rapid luciferase should increase their use, especially in but not very specific. The bacterial luminescent food microbiology. These assays will not eliminate assays are rapid – fast enough for near on-line the classical microbiological methods, but they assays that require an immediate action, such as will enhance the importance of microbial assays the detection of antimicrobials in milk. The speed in areas such as the HACCP system where rapid of detection may also, in some cases, reduce the results are necessary. The advancements in genetic costs. The method is simple enough to use so that engineering of microorganisms aimed at making plant workers could perform the test. It is sensi- them bioluminescent, coupled with a need for tive – very low numbers of cells can be detected rapid microbiological assays in the food industry, with luminometers and the continued research will make in vivo bioluminescence a common may lower those numbers even further. In most practice in the future. Bioluminescence, together cases it is advantageous that the in vivo biolumi- with low level light detection systems such as nescence assay is noninvasive. No cell disruption photon counting and CCD imaging, will provide is required to measure the light emission. It has the food microbiologist with a very powerful tool been shown to be an accurate method exhibiting for studying food as an , and will offer a good correlation with the cell counts – for both unique opportunity to study microbial behaviour increasing and decreasing numbers. and interactions in food. When using narrow range phages to introduce the lux genes, assays can be specific to detect a Acknowledgement. We are grateful to Prof. ISRAEL GOLD- particular organism. A final advantage is that the BERG from the Hebrew University of Jerusalem for critical technology of bacterial bioluminescence leads to reading of the manuscript. The main part was done in the a great deal of innovations in many areas. As with frame of the First International Postgraduate Course on Food any new technique, it also has disadvantages. There Technology held in Hebrew University of Jerusalem, Faculty could be a problem with phage or plasmid host of Agriculture, Division for External Studies, Rehovot, Israel. ranges being either too specific or too wide, result- ing in false negatives or false positives, respectively. Reference s Another disadvantage to the food microbiology industry is that the bacterial bioluminescent assays ANONYM (1996): Lumac Beer Microbial Kit, Lumac Hy- are still at the experimental and prototype stages, giene Monitoring Kit, Lumac Meat Microbial Kit, Lumac in contrast to the ATP bioluminescent assay. Raw Milk Microbial Kit, Lumac Water Microbial Kit. There are also general disadvantages with the Technical Specifications, Perstorp Analytical Lumac, luminescent methods. The principal disadvantage is Landgraaf, the Netherlands. the quenching of emitted light that can adversely af- BAKER J.M., GRIFFITHS M.W., COLLINS-THOMPSON D.L. fect the measurements. Namely certain compounds (1992): Bacterial bioluminescence: Applications in food from the biological samples can strongly reduce the microbiology. Journal of Food Protection, 55: 62–70. amount of the light measured photometrically. On BASOL M.S., GOGUS U. (1996): Methods of antibiotic the other hand, there are some luminescent non- applications related to microbiological quality of lamb microbial substances in the biological samples that by PCA and bioluminescence. Journal of Food Science, can increase the intensity of the measured light. 61: 348–349, 356. BAUMAN H.E. (1974): The HACCP concept and micro- CONCLUSION biological hazard categories. Food Technology, 28: 30, 32, 34, 74. A great deal of research in the last 30 years has BAUTISTA D.A., VAILLANCOURT J.P., CLARKE R.A., been directed towards the development of the RENWICK S., GRIFFITHS M.W. (1994): Adenosine tri-

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Corresponding author

Ing. PAVEL DOSTÁLEK, CSc., Vysoká škola chemicko-technologická, Fakulta potravinářské a biochemické technologie, Ústav kvasné chemie a bioinženýrství, Technická 5, 166 28 Praha 6, Česká republika tel.: + 420 220 444 037, fax: + 420 220 445 051, e-mail: [email protected]

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